First Record of the Bush-Cricket Isophya Harzi (Orthoptera: Phaneropteridae) Outside Its Locus Typicus

Travaux du Muséum National d’Histoire Naturelle © 28 décembre «Grigore Antipa» Vol. LV (2) pp. 201–206 2012 DOI: 10.2478/v10191-012-0011-0

FIRST RECORD OF THE BUSH-CRICKET ISOPHYA HARZI (ORTHOPTERA: PHANEROPTERIDAE) OUTSIDE ITS LOCUS TYPICUS

IONUŢ ŞTEFAN IORGU, ALEXANDRU IOAN TATU, ELENA IULIA IORGU

Abstract. During the period 2008-2012, the bush-cricket Isophya harzi Kis, 1960 has been the subject of several collecting trips in Cozia Mountains, where it was believed to be endemic, in order to study its acoustic behaviour. However, on a recent trip to Piatra Craiului Mountains, to study its Orthoptera fauna, I. harzi was surprisingly found in clearings and mountain steppe slopes covered with tall subalpine vegetation from Northern and Western areas. Bioacoustic analysis and some ecological notes are presented in the paper.

Résumé. La sauterelle Isophya harzi Kis, 1960 a été l’objet de plusieurs voyages de collecte dans les Montagnes de Cozia, pendant 2008-2012, afin d’étudier son comportement acoustique. Lors d’une etude récente sur la faune des Orthoptères des montagnes Piatra Craiului, I. harzi a été trouvée avec surprise dans les clairières et sur les pentes couvertes de steppes subalpines dans les régions nord et ouest de la montagne. L’analyse bioacoustique et quelques notes écologiques sont présentées.

Key words: Isophya harzi, distribution, Romania, bioacoustics.

INTRODUCTION Genus Isophya Brunner von Wattenwyl is one of the largest of Palaearctic Orthoptera, with about 90 species known so far (Eades et al., 2012). Many of these bush-crickets have small distributional area, some of them being considered endemic species, characterized by limited mobility and usually confined to specific topographic requirements (Sevgili et al., 2006; Chobanov, 2009). They are usually found in small, isolated populations with a low density. Partly due to their preference to feed on dicotyledonous plants, they have a strict habitat preference (Bauer & Kenyeres, 2006). The study of this genus in the Carpathians can help elucidate some of the zoogeographical processes occurring after the last ice age (Kenyeres et al., 2009). Isophya harzi Kis, 1960, one of the few Orthoptera species listed on both IUCN Red List of Threatened Species and Annex II from Habitats Directive, occurs in the Southern Carpathians, Romania. Up to this study, it was supposed to be endemic to a small area from Cozia Mountains, from where it was described in 1960 by Béla Kis. Kenyeres et al. (2009) postulate that this species is a recently isolated endemism and survived the last glaciation in situ. The species’ song has been described recently by Orci et al. (2010), thus helping the clarification of its taxonomic status and allowing an easier identification of specimens directly on the field. Our finding of the species in Piatra Craiului Mountains, more than 65 km away in a straight line, supports the importance of knowing the species distribution in its conservation efforts. Its presence in other mountains from Southern Carpathians is very likely, because of similarities in habitat conditions. 202 IONUŢ ŞTEFAN IORGU, ALEXANDRU IOAN TATU, ELENA IULIA IORGU

MATERIAL AND METHODS During several expeditions in Cozia Mountains in the period 2008-2012 and one trip in Piatra Craiului Mountains in July 2012, several specimens of Isophya harzi were caught alive in order to study their acoustic behaviour. Males and females

c Fig. 1 - Isophya harzi: a, habitat; b, ♂; c, ♀ (Piatra Craiului Mts., 29.07.2012; photos: I. Şt. Iorgu). ISOPHYA HARZI (ORTHOPTERA) OUTSIDE LOCUS TYPICUS 203 have been recorded indoors, using the digital recorder EDIROL R-09HR and directly in the field, using the same recorder and the external microphone EDIROL CS-15R attached. Photos and tegminae movements while producing sounds were recorded with a Canon DSLR EOS 600D and a Canon 100 mm 2.8 1:1 macro lens. Song terminology follows Heller et al. (2004) and Orci et al. (2010). Sound analysis was performed with Audacity 2.0.2.

RESULTS AND DISCUSSIONS Order Orthoptera Suborder Ensifera Family Phaneropteridae Isophya harzi Kis, 1960 (Figs 1 a-c; 2 a-f; 3 a-g) Examined material. 6 ♂♂, 4 ♀♀, 19.08.2008, Cozia Mts., 45°18.86’N, 24°20.76’E, 1380 m, leg. I. Şt. Iorgu & E. I. Iorgu; 6 ♂♂, 4 ♀♀, 01.08.2009, Cozia Mts., 45°19.06’N, 24°20.31’E, 1580 m, leg. I. Şt. Iorgu; 10 ♂♂, 7 ♀♀, 17.08.2010, Cozia Mts., 45°19.04’N, 24°20.42’E, 1590 m, leg. I. Şt. Iorgu & E. I. Iorgu; 8 ♂♂, 6 ♀♀, 29.07.2012, Piatra Craiului Mts., 45°33.49’N, 25°14.40’E, 1380 m, leg. I. Şt. Iorgu & A. I. Tatu; 2 ♂♂, 1 ♀, 29.07.2012, Piatra Craiului Mts., 45°33.19’N, 25°14.68’E, 1930 m, leg. I. Şt. Iorgu; 3 ♂♂, 29.07.2012, Piatra Craiului Mts., 45°31.89’N, 25°11.76’E, 1420 m, leg. I. Şt. Iorgu; 2 ♂♂, 2 ♀♀, 30.07.2012, Cozia Mts., 45°18.82’N, 24°22.62’E, 1030 m, leg. I. Şt. Iorgu. Audio recordings. 3 ♂♂, 01.08.2009, Cozia Mts., air temperature 26ºC; 7 ♂♂, 3 ♀♀, 17.08.2010, Cozia Mts., air temperature 25ºC; 4 ♂♂, 29.07.2012, Piatra Craiului Mts., air temperature 19ºC; 2 ♂♂, 30.07.2012, Cozia Mts., air temperature 19ºC. Bioacoustics. The bush-cricket Isophya harzi stridulates at dusk and during the night. Male calling song consists of temporal variable groups of syllables (for more details see Orci et al., 2010). A group is well defined in structure, two types

Table 1 Song characteristics of Isophya harzi (n = number of recorded males, t = temperature). Male song Min. Max. Mean SD n t (ºC) Syllable duration (ms) 75 168 121.64 28.36 Number of impulses 23 55 40.5 9.67 Short (“A”) syllable Delay of after-clicks (ms) 40 90 64 16.97 Number of after-clicks 0–2 Syllable duration (when producing after-clicks) 75 258 156.42 77.01 Gap between consecutive short (“A”) syllables (ms) 122 298 175.78 48.25 Gap between short (“A”) and long (“B”) syllables (ms) 367 789 527.4 126.18 16 19–26 Syllable duration (ms) 94 216 154.7 43.54 Number of impulses 37 59 46.5 8.38 Long (“B”) syllable Delay of after-clicks (ms) 75 202 142.3 47.19 Number of after-clicks 0–2 Syllable duration (when producing after-clicks) 94 418 223.3 114.78 Syllable group total duration (ms) 617 6168 2254.8 1954.04 Gap between consecutive syllable groups (ms) 191 303 249.8 40.28 204 IONUŢ ŞTEFAN IORGU, ALEXANDRU IOAN TATU, ELENA IULIA IORGU

Fig. 2 - Sound analysis in Isophya harzi: a, oscillogram - male calling song, Piatra Craiului Mts., temperature 19ºC; b, oscillogram - male calling song, Cozia Mts., temperature 19ºC; c, d, oscillogram - detailed group of syllables: first two syllables short (“A”), last one long (“B”); e, oscillogram - male - female acoustic duet, Cozia Mts., temperature 25ºC; f, spectrum - red, Piatra Craiului Mts.; green, Cozia Mts. of syllables being produced: a sequence of 1-36 short (“A”-type) syllables (usually 2-6), followed by a long syllable (“B”-type). Very interesting is that the gap between successive “A” and “B” syllable is longer than the gap between “B” and consecutive “A” syllable, creating the false impression that the group actually begins with “B” syllable. The groups of syllables are produced in sequences, from 2 to more than 20 groups being produced without gaps longer than 303 ms between consecutive ones. Usually, the last group in a sequence lacks the ending long syllable (Fig. 2 a, b). The “A”-type syllables are formed of 23-55 impulses lasting for 75-168 ms, sometimes after-clicks being produced after 40-90 ms. The “B”-type syllable consists of 37-59 ISOPHYA HARZI (ORTHOPTERA) OUTSIDE LOCUS TYPICUS 205

Fig. 3 - Distribution map of Isophya harzi in Romania: a, Cozia Mts. (45°19.06’N, 24°20.31’E); b, Cozia Mts. (45°18.86’N, 24°20.76’E); c, Cozia Mts. (45°19.04’N, 24°20.42’E); d, Cozia Mts. (45°18.82’N, 24°22.62’E); e, Piatra Craiului Mts. (45°31.89’N, 25°11.76’E); f, Piatra Craiului Mts. (45°33.19’N, 25°14.68’E); g, Piatra Craiului Mts. (45°33.49’N, 25°14.40’E). impulses and lasts for 94-216 ms. The after-clicks, if present after “B” syllables, are produced after 75-202 ms (Fig. 2 c, d). When willing to mate with the singing male, female replies with a short song formed of isolated impulses and produced only after the beginning of male “B” syllable, sometimes overlapping with male syllable main body (Fig. 2 e). This proves that male groups begin with the series of “A” syllables and end with “B” syllable, as females reply usually to a (ending) trigger element, in this case the long syllable (Orci et al., 2010). The song frequency ranges from 10 kHz up to 30-40 kHz, with the highest peak recorded at about 19-22 kHz (Fig. 2 f). Ecology and distribution. This bush-cricket inhabits sunny mesophytic forest ecotones and growth clearings, subalpine grasslands, abundant in Rubus, Urtica, Rumex, Veratrum, Aconitum, Vaccinium etc. It is distributed over a wide range of altitudes, from 1000-1600 m altitude in Cozia Mountains and from 1400 m up to more than 1900 m in Piatra Craiului. It may well be that Isophya harzi’s distribution area includes more mountain massifs between Olt and Prahova river valleys, as this area is still in need of a thorough research (Fig. 3). In the course of time, new protected areas (European Commission Habitats Directive Sites of Community Importance) may be designated on the presence of this particular bush- cricket in the Southern Carpathians and checklists should be updated in already nominated Sites of Community Importance.

ACKNOWLEDGEMENTS The authors acknowledge Adrian Derscariu and Irinel Popescu, their traveling companions in the Carpathian Mountains. We are grateful to anonymous reviewers for improving the paper. 206 IONUŢ ŞTEFAN IORGU, ALEXANDRU IOAN TATU, ELENA IULIA IORGU

PRIMA SEMNALARE A COSAŞULUI ISOPHYA HARZI (ORTHOPTERA: PHANEROPTERIDAE) ÎN AFARA LOCUS TYPICUS REZUMAT Cosaşul Isophya harzi Kis, 1960 a fost subiectul mai multor excursii de colectare în Munţii Cozia, în perioada 2008-2012, pentru a-i studia comportamentul acustic. În timpul unui studiu recent în Munţii Piatra Craiului, I. harzi a fost găsită în mod surprinzător în poienile şi zonele cu vegetaţie subalpină de pe stâncăriile abrupte din nordul şi vestul masivului. În lucrare sunt prezentate analiza bioacusticii şi câteva date ecologice.

LITERATURE CITED BAUER, N., Z. KENYERES, 2006 - Habitat preference studies of some species of the genus Isophya Brunner von Wattenwyl, 1878 (Orthoptera: Phaneropteridae) in the Western part of the Carpathian Basin. Journal of Orthoptera Research, 15 (2): 175-185. CHOBANOV, D. P., 2009 - Phylogeny and systematics of the Isophya modesta group (Phaneropteridae) based on morphology and bioacoustics. Metaleptea, 29: 20-27. EADES, D. C., D. OTTE, M. M. CIGLIANO, H. BRAUN, 2012 - Orthoptera Species File Online. Version 2.0/41. http://Orthoptera.SpeciesFile.org (accessed at 11 October 2012). HELLER, K.-G., K. M. ORCI, G. GREIN, S. INGRISCH, 2004 - The Isophya species of Central and Western Europe (Orthoptera: Tettigonioidea: Phaneropteridae). Tijdschrift voor Entomologie, 147: 237-258. KENYERES, Z., I. A. RÁCZ, Z. VARGA, 2009 - Endemism hot spots, core areas and disjunctions in European Orthoptera. Acta zoologica cracoviensia, 52 B (1-2): 189-211. KIS, B., 1960 - Revision der in Rumänien vorkommenden Isophya - Arten (Orthoptera, Phaneropterinae). Acta Zoologica Academiae Scientiarum Hungaricae, 6 (3-4): 349-369. ORCI, K. M., G. SZÖVÉNYI, B. NAGY, 2010 - A characterization of the pair forming acoustic signals of Isophya harzi (Orthoptera, Tettigonioidea, Phaneropteridae). Acta Zoologica Academiae Scientiarum Hungaricae, 56 (1): 43-53. SEVGILI, H., B. ÇIPLAK, K.-G. HELLER, A. DEMIRSOY, 2006 - Morphology, bioacoustics and phylogeography of the Isophya major group (Orthoptera: Tettigoniidae: Phaneropterinae): a species complex occurring in Anatolia and Cyprus. European Journal of Entomology, 103 (3): 657-671.

Received: November 7, 2012 Ionuţ Ştefan Iorgu, Elena Iulia Iorgu Accepted: December 18, 2012 “Grigore Antipa” National Museum of Natural History Şos. Kiseleff 1, 011341 Bucharest 2, Romania e-mails: [email protected] [email protected] Alexandru Ioan Tatu “Babeş-Bolyai” University, Department of Taxonomy and Ecology, Str. Clinicilor no. 5-7, 400006 Cluj-Napoca, Romania e-mail: [email protected]